Abstract

Path integration is a fundamental skill for navigation in both humans and animals. Despite recent advances in unraveling the neural basis of path integration in animal models, relatively little is known about how path integration operates at a neural level in humans. Previous attempts to characterize the neural mechanisms used by humans to visually path integrate have suggested a central role of the hippocampus in allowing accurate performance, broadly resembling results from animal data. However, in recent years both the central role of the hippocampus and the perspective that animals and humans share similar neural mechanisms for path integration has come into question. The present study uses a data driven analysis to investigate the neural systems engaged during visual path integration in humans, allowing for an unbiased estimate of neural activity across the entire brain. Our results suggest that humans employ common task control, attention and spatial working memory systems across a frontoparietal network during path integration. However, individuals differed in how these systems are configured into functional networks. High performing individuals were found to more broadly express spatial working memory systems in prefrontal cortex, while low performing individuals engaged an allocentric memory system based primarily in the medial occipito-temporal region. These findings suggest that visual path integration in humans over short distances can operate through a spatial working memory system engaging primarily the prefrontal cortex and that the differential configuration of memory systems recruited by task control networks may help explain individual biases in spatial learning strategies.

Highlights

  • Humans and animals are able to spatially code their movement through environments using a combination of visual optic flow and self-motion cues (Mittelstaedt and Mittelstaedt, 1980; Etienne and Jeffery, 2004; Sargolini, 2006; Wolbers and Hegarty, 2010)

  • NEURAL BASIS OF VISUAL PATH INTEGRATION – TASK partial least squares (PLS) A task PLS analysis was carried out to identify the brain regions that were engaged by the entire group during all path integration trials regardless of accuracy

  • Dominant positive voxel saliences with a Bootstrap ratios (BSRs) of 4.5 (p < 0.0001) indicating brain regions showing significant increases in blood oxygen level dependent (BOLD) signal during the path integration task were found bilaterally in the inferior parietal lobe (IPL) extending into the intraparietal sulcus (IPS), middle (MFG) and superior frontal gyrus (SFG), anterior insula (AI), and precentral gyrus, as well as the right rolandic operculum, precuneus, and the left cerebellum. These regions suggest the engagement of topdown control systems (Dosenbach et al, 2008; Cole et al, 2013) that interact with spatial attention (Kastner and Ungerleider, 2000; Corbetta and Shulman, 2002; Silk et al, 2010) and working memory (Haxby et al, 2000; Müller and Knight, 2006; Ikkai and Curtis, 2011) systems to initiate attentional control toward the optic flow cues needed to monitor, store and evaluate metric and angular displacement within the virtual environment

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Summary

Introduction

Humans and animals are able to spatially code their movement through environments using a combination of visual optic flow and self-motion cues (Mittelstaedt and Mittelstaedt, 1980; Etienne and Jeffery, 2004; Sargolini, 2006; Wolbers and Hegarty, 2010) This process is known as path integration, or dead reckoning, and is widely believed to be a fundamental navigational skill used to estimate self-location in an environment by tracking distances and directions from a given reference point. Despite having numerous scientific implications, to date there has been little interest in understanding how path integration operates in humans at a neural level

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